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Arbuscular Mycorrhiza and Soil Microbes

Mohammad Miransari
Department of Soil Science, College of Agricultural Sciences Shahed University, Tehran, Iran

Introduction
Soil rhizosphere is a very interesting and complicated environment surrounding plant roots. There are very many different types of microorganisms in the soil rhizosphere interacting with the other microbes and with plant roots. The properties of soil rhizosphere make it a unique and active area. The activity and interactions of rhizotrophic microorganisms can very much influence soil conditions and hence plant growth and microorganism activities [1]. Arbuscular mycorrhizas (AM) are among the most important and influencing soil microbes significantly affecting the growth of plants and other soil microorganisms. The soil part around the plant roots and AM hypha, where AM and bacteria are interactive is called mycorrhizosphere. There are also different types of soil bacteria in the soil, which are interactive with AM, particularly in the rhizosphere and in most cases the interactions are synergistic. Consideration of the rhizotrophic interactions and their consequent effects on the soil properties and hence plant growth can have very important implications in agriculture and ecology. There are different effects resulted by such interactions, which modified soil structural properties [2] and soil enhanced availability of nutrients [3] are among the most important ones. Thus, it is pertinent to evaluate such interactions precisely and suggest some new perspectives for the future research, which can make the advance of the field more rapidly and result in more efficient agricultural strategies.

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M. Miransari

Arbuscular Mycorrhiza
Arbuscular mycorrhiza (AM) are zygomycetes belonging to the order Glomales. According to both fossil discoveries and DNA sequences, the appearance of both AM and plants is almost 400 million years old [4]. AM are able to develop symbiotic association with most terrestrial plants [5-8] and usually their symbiosis with the host plant is not host specific. In their symbiosis, the host plants provide the fungi with their required hydrocarbon and receive nutrients, especially P from the fungi [6, 9, 10]. The passage of AM into the plant roots is through their hypha, which would eventually form the arbuscules and the vesicles. Arbuscules are branched structural hypha, which are the place of nutrient exchange with the plant roots. Vesicles are the specialized storage organelles with numerous and large vacuoles, which can greatly help the host plant especially under different stresses such as salinity and heavy metals. The onset of the symbiosis and the beneficial effects of the two symbionts become likely through the communication of some signal molecules [9, 11]. AM are able to enhance plant tolerance to different stresses such as soil salinity and drought, soil compaction, heavy metals and pathogens [12-19]. Plant responses to different species of AM are different, and since AM greatly affect the variousness, biomass and nutrients uptake of plants, AM species determine very much the structure of plant communities [20, 21]. Different efficiency of plants species in symbiosis with AM species affects their ecological functioning [5, 12, 18-22]. AM is able to greatly influence plants structure, hence combination recognition of AM species, in symbiosis with plant species is very important. Although the AM-plant symbiosis is not specific, the probability of some symbiotic combinations is more likely. Compared with other AM-plant symbiosis some combinations are more common under field conditions [21].

Arbuscular Mycorrhiza and Soil Bacteria

Although AM are very important symbionts to plants and their symbiosis can significantly enhance the growth of the host plant, they are also very much interactive with different bacteria including both the bacterial strains in the rhizosphere and in the bacterial strains in the cytoplasm of some fungal species [23]. Understanding such interactions, particularly in agricultural producing areas with not much resources of input is of great significance and is a very interesting research topic, and in the meanwhile complicated, in the field of molecular microbe-plant interactions [23]. Relative to the complete recognition of symbiotic stages, activated during the process of N fixation between rhizobium and the specific host plant, including the exchange of the signal molecules between the two partners [24, 25], there are much more details, which should yet be elucidated regarding the symbiosis of AM with the host plant [23].
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However, it should be mentioned that some very interesting achievements regarding the establishment of symbiosis between AM and the host plant including the recognition of the signal molecules involved, have been recently achieved [26]. In addition, the recognition of genes such as phosphate transporter genes [27] and metallothionein producing genes [28] related to the functional properties of AM are of great significance. The obstacles related to mycorrhizal research including their mandatory biotrophic nature, their cellular structure and their variable genetical properties have made the advance of the field less rapid, relative to the rhizobium-legume symbiosis [23, 29]. In addition to the large size of AM genome (0.3 pg to 1.12 pg/DNA) that has made the performance of AM genomic projects unlikely [23]; the significance of the host plant should also be noticed. It is because the first plant that has been genetically sequenced is Arabidopsis thaliana, which is not a host to AM [30]. However, plants including rice are host to AM and, hence, the research related to rice genomic data can illustrate some very important knowledge regarding AM symbiosis [31]. Different researches have indicated that there are about 100,000 genes related to AM plant host symbiosis. Additionally, using mutants have indicated the presence of proteins, which are communicated between the two partners at the time of symbiosis establishment [32]. Also the discovery of genes such as NORK and SYMRK have made the identification of pathways related to signal perception by the host plant and bacteria and AM likely [23]. Arbuscular mycorrhiza are also great niches for other soil microbes and while some of the bacteria are attached to AM hypha, some of them are bound to plant roots [33, 34]. While for other eukaryotic cells the association with bacteria is very common [35], for AM fungi only a few strains of bacteria are integrated into the fungi [36, 37]. There are bacterial-like structures in the cytoplasm of AM [38, 39]. The presence of bacteria in AM species taken from the field has been indicated by ultra structural ways. It is very important to determine the bacterial population, associated with AM fungi, with the highest physiological activities. This indicates the bacterial strains that are more efficient, particularly when interactive with AM, and can make the use of effective co-inoculation likely. There are different methods for the determination of bacterial association with AM. For example, for tagging and visualizing the bacterial strain Paenibacillus brasilensis, which has suppressing effects on the activity of plant pathogens and can stimulate the activity of some specific AM species, von der Weid et al. [40] used the green fluorescence protein technique. Arbuscular mycorrhiza and bacterial interactions can take place in the rhizosphere before the onset of inoculation or after the establishment of the tripartite symbiosis between AM, bacteria and the host plant [39]. The synergistic interactions of AM and bacteria can stimulate plant growth through enhancing processes such as nutrients uptake and controlling plant pathogens. These processes are of great significance, especially in agricultural cropping
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M. Miransari

strategies, which are not depending much on agrochemicals to maintain soil fertility and health. In addition, AM are also able to influence the combinations of soil bacterial populations [41]. These effects can be related to the alteration of root physiology by affecting the chemical combination of root products [42, 43]. Additionally, AM can also alter the combination of bacteria in the rhizosphere through competition for soil nutrients [44]. Scientists have also stated that the association of some bacteria with AM is specific [41] indicating that there are some kind of communications between the bacteria and AM, stimulated by fungus exudates [39]. This is also verified by the results of scientists who found that some bacterial genera including Arthrobacter and Bacillus were most common in the hyphosphere or the soil around specific AM hypha, while Pseudomonas spp. were most distributed in the Sorghum bicolour rhizosphere. This suggests that the likelihood of Gram-positive bacterial association with AM is higher related to the Gram-negative bacteria, but has yet to be verified [41]. Additionally, it has been stated that bacterial genera are more frequent in the rhizosphere than hyphosphere indicating that root exudates can be more beneficial to the bacteria than hyphal products [39]. There are different examples of enhancing association between bacteria and AM including species of Bacillus, Paenibacillus, Pseudomonas and Rhizobia that are in association with AM species of Glomus including G. calrum, G. intraradices, G. mosseae, G. versiforme, and G. intraradices. These stimulating effects include the growth and germination of fungi and spores, respectively, root colonization of the host plant by AM, the solubilization of phosphate, and the suppression of pathogens [39]. The significance of bacterial attachment to the AM hypha and whether it can affect hyphal growth has yet to be elucidated. However, if this is the case, the co-inoculation of appropriate bacteria with AM can significantly contribute to enhanced plant growth [39]. In addition to the nutritional effects of fungal products on bacterial growth, production of glycoproteins such as glomalin can also influence bacterial growth in the soil through improving soil structure [2]. For example, the bacteria, present in the water soluble aggregates are different from the bacteria, present in the non-soil water aggregates [39]. Bacterial types, which are interactive with AM, are saprophytes and symbionts that some of which are unfavourable, some are neutral and some are favourable [45]. The bacteria that are able to enhance plant growth through interacting with plant roots are called plant growth promoting rhizobacteria (PGPR). Although it has been indicated that some of the PGPR are able to perfectly inoculate plant roots, data related to the inoculation intensity of AM hypha by PGPR is little. According to Bianciotto et al. [46] the intensity attachment of some species of Rhizobium and Pseudomonas to AM germinating spore and
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hypha under sterilized conditions was different depending on the strains of bacteria. However, the level of specificity was not recognized. The strength of bacterial binding to AM hypha differs during the different physiological stages of attachment including a weak electrostatic attachment in the first stage followed by a strong attachment in the second stage, which is related to the production of cellulose or other extracellular products by bacteria. This hypothesis is supported by the less strong attachment of bacterial mutants, which were not able to produce such products, to the AM hypha [39]. Because some bacterial strains such as Pseudomonas spp. are able to colonize both plant roots and AM hypha, it has been suggested that the related processes can be relatively similar. Although, there has been a lot of research on the interactive activities between AM and bacteria, more research should be conducted to more clearly elucidate the processes involved in the interactions between AM and soil bacteria. This can be very useful for the optimum determination of bioinoculants, necessary for sustainable agricultural cropping strategies [39]. In addition to the stimulating effects of PGPR on plant growth through enhancing nutrients uptake, suppressing pathogens and some beneficial biochemicals, their interactive effects with AM can also increase plant growth [39]. Researchers have stated that PGPR can have some very stimulatory effects on AM growth [47]. This indicates that the co-inoculation of AM and specific PGPR can enhance the activity of AM during the symbiosis with the host plant [39]. This is because for example, some PGPR such as Pseudomonas putida are able to stimulate the root inoculation of host plants by AM [48]. The interaction between AM and bacteria, particularly PGPR [49, 50], and N-fixing bacteria are very beneficial to the host plants. The data regarding the simultaneous and enhancing effects of AM and PGPR on plant growth is little. It has just been recently that these effects have been tested, simultaneously [39]. Some of the bacteria are able to influence AM activity of spore germination and growth rate [51, 52] and hence affecting plant growth through AM symbiosis.

Arbuscular Mycorrhiza and N-fixing Bacteria

Unlike AM, which develop symbiosis with most terrestrial plants, N-fixing bacteria are able to establish symbiotic association with their specific host plant and fix atmospheric N [4, 21, 24, 25, 53]. The N-fixing bacterial symbionts including the genera Azorhizobium, Bradyrhizobium, Mezorhizobium, Rhizobium and Sinorhizobium, collectively called rhizobia, are settled in a plant membrane including compartment called symbiosome [4, 54]. Similar to AM-plant symbiosis the bacteria-legume symbiosis is also of very important agricultural and environmental implications, because it can substantially contribute to N production and utilization [55, 56].
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Process of N Fixation
Through some very interesting and in the meanwhile complicated biochemical dialogue, the bacteria realize the presence of the specific host plant roots and chemotactically approach the plant roots. The stages related to the development of symbiosis between the N-fixing bacteria and the host plant include: the root exudation of signal molecules, the gene activation of bacteria by the exudates [24, 25] and production of some biochemicals by the bacteria [57] that can induce morphogenesis and physiological changes in the host roots. This eventually results in the formation of nodules, which are the place of bacterial settlement and hence N fixation [24, 25]. Although N fixation by rhizobial symbiosis supplies the host plant with additional N, high amounts of energy and P must be available to the symbiosis process [21]. Different species of AM are able to provide the host plant with various amounts of P [58-60]. Arbuscular mycorrhiza are also able to mineralize organic N in the mycorrhizosphere and increase N availability to the plant [39]. It is believed that the N-fixing capability of Rhizobium may enhance if the host plant is also in symbiosis with AM. Under such a situation and with regard to enhancing the colonization rate, uptake of inorganic nutrients and plant growth, Rhizobium and AM are synergistic [39]. There are some common genetical stages for both bacterial N fixation and AM symbiosis. The extent of plant accommodation for the intracellular settlement of endosymbionts including AM and bacteria has yet to be recognized [4]. Accordingly, there are some differences between the bacteria and AM for the preparation of the symbiosis with their partner. For example, the weakening strength of the root cell walls for the passage of the bacteria into the roots is not common for AM passage into the roots [4]. Legumes may prefer to develop symbiosis with AM species, which are more efficient to supply P. This can be very advantageous under the conditions that nutrients are not available at high amounts [61]. Different AM species are able to increase nodulation and N fixation differently [21, 62]. The beneficial effect of AM on P uptake by Rhizobium has been proved through providing the non-mycorrhizal plants with additional P resulting in enhanced plant growth, which is comparable with the growth of mycorrhizal plants [39, 60]. The researches regarding AM variousness in legumes and their colonization of legume nodules are not much. Scientists have indicated that AM are able to colonize root nodules in the laboratory [63]. However, nodules colonization of AM under field conditions and the species of AM, which are able to colonize legumes nodules, is yet to be recognized. The structure, functioning, and nutritional demand of nodules are different with plant roots. Nodules are produced by cortical cell division, in which rhizobia with high energy and P requirements reside and fix N [21].
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Nodule formation also alters plant physiological properties and induces plant systematic acquired resistance [21, 64] suggesting that AM species combination may be different in roots and nodules. AM communities in legume roots are different with non-legume roots. Some AM species are able to develop symbiosis with plants containing high amounts of N. This is also in agreement with the finding that N fertilization can alter the combination of AM species and also with the finding that the level of G. intraradices with the Glo8 sequence type increased, after fertilization with N and P fertilizers [65]. While N-fixing bacteria utilize dicarboxylates as their source of energy [66], AM absorb [67] glucose and fructose, just when residing in plant roots, and hence hexoses are translocated to the AM fungi [10]. Endosymbiosis is accompanied with the production of a high amount of symbiosome membrane, for example the area of plasmamembrane for a nodule cell with bacteroids is about 2800 M2, however the area for the symbiosome membrane is 21,500 M2 [68]. Additionally, since different nutrients must be translocated into the cells containing the symbionts, different compositions of proteins including different transporters are located within the symbiosome membrane. Also the prebacteroid [69] and the prearbuscular membranes have ATPase activities, which are not available in pathogenic interactions [70]. Thus, the symbiosome membrane form two different components, one for the inclusion of the symbionts and one for the control of different proteins compositions and their activities. While the mutants of Bradyrhizobium japonicum are not able to activate under low oxygen conditions, the bacteria is able to develop a mechanism by which they can be active and fix N [71] under such conditions. Different mutants are categorized based on lacking the ability to synthesize cytochromes (necessary for bacteroids formation), pass through the infection thread, and transcribe different plant genes necessary for nodulins formation [72]. The symbiosis of AM species with legume plants make them more efficient, for example through enhancing nutrient uptake such as P, Cu and Zn, which are very important for nodulation and N fixation. Hence, the specificity between AM, and its host plant can be very important, as legumes would develop symbiosis with AM species, which are more efficient [21]. The tripartite symbiosis between AM, bacteria and legumes is of great significance both for agriculture and for ecology, and scientists have been trying to find the most efficient combination of AM and bacteria [21]. Although the colonization of legume nodules by AM have been proved in the laboratory, there is very little relevant data under field conditions. Compared with plant roots, the combination of AM species was unique for legume nodules; however the combination was similar for three different legume species. Although sequence type Glo8 was found more in legume nodules, sequence type Acau5 was just found in legume nodules. It is also worth mentioning that legume roots exclusively contained sequence type 50. These all suggest that legume nodules may have enhancing or inhibiting effects on root colonization of some AM species [21].
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The following reasons indicate the specificity of legume nodules in their association with AM species: (1) the high tendency of nodules for nutrients such as P, Cu or Zn, might result in the association of some AM species with legume nodules, (2) high nodule N concentration may be preferable to some AM species (for example AM species with Glo8 and Acau5 sequences), (3) the similarities between the stages of nodule and AM symbiosis, as there are some very important common stages [21, 22] and hence, legume mutants, which are not able to develop symbioses with rhizobia, may not also develop symbioses with AM species [73], (4) AM symbiosis development is influenced by rhizobial signals [74], and (5) the different physiology of nodules and roots and also the alteration of root exudates by rhizobial symbiosis and the induction of systematic acquired resistance in plants. These are all the likely explanations indicating the different tendency of root nodules for different AM species as all affect the ability of AM species to colonize legume nodules [21]. They also found that AM species isolated from the field were able to colonize legume nodules by forming hypha around the nodules and producing hypha and spores in the nodules. Plant host species determine the combination of AM species in legume roots indicating that the tendency of different host plants for symbiosis development with different AM species differs. Some AM species (with Glo8 and Glo3 sequences) have the ability to colonize a wide range of host legume plants in both roots and nodules [75]. Using the same PCR methods the variousness of AM species ranged from 0.4 to 2.3, using the Shannon index under cultivated field and tropical rain forest conditions [76]. The parameter most influencing the Shannon index is the specific plant species rather than the number of plant species. Hence, parameters such as the nature of plants functionality (legumes or non-legumes), species of plants and root components including roots and nodules can determine AM communities in plants. More research is required to specify the effects of different AM species combinations on plant and nodule performance, and also on the structure and combination of plants [21]. Seed inoculation of legumes with N-fixing bacteria including rhizobia and bradyrhizobium can be of some very practical applications as the method has turned into a very useful applicable technology in both developed and developing countries [77]. The environmental and economical approaches of N fixation are also very significant, as for example by application of less N fertilizer and the beneficial interacting effects of bacteria with other soil microorganisms including AM. As previously mentioned usually legume plants are able to make tripartite symbiosis with N-fixing bacteria and AM. This kind of association can be very beneficial both to the plant and to the symbiotic microbes. To make the tripartite symbiosis highly efficient the interactions between the plants, the bacteria and the AM must exactly be elucidated. Scientists [78, 79] have indicated some interesting aspects related to such kind of symbiosis.
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However, almost few researches have indicated the beneficial effects of AM, both local and inoculated on bacteria-legumes symbiosis. AM are able to transfer the absorbed N from the soil to the plant. It has been stated that AM are able to mineralize organic N present in organic matter and hence make soil N more available to the bacteria interactive with AM. However, the organic matter utilizing and mineralizing by AM and hence plant and AM nutrient uptake, which is related to the stimulating effects of AM on mineralizing bacteria, has yet to be elucidated [80]. The network of mycorrhizal hypha are able to transfer N between and within the plants. In addition to the important role of AM in cycling the nutrients, their contribution to intensive agriculture should also be clearly indicated [7]. By enhancing N uptake and hence plant growth and also through affecting bacterial dependence on atmospheric N, AM may affect N fixation. Under non-sterile conditions, legume roots can develop symbiosis with AM, which can help the plants such as forage and crop legumes absorb higher rate of N. AM and rhizobium can synergistically and significantly affect the symbiotic related parameters [7]. The different responses of legume species to AM inoculation have also been attributed to different root morphology and architecture and also different dependency on AM [81]. Compared with control, AM inoculation, plant dry matter, fixed N, P and K uptake were significantly increased in different varieties of Phaseolus vulgaris and Vicia faba, inoculated with a mixture of R. leguminosarum bv. phaseoli and R. tropici and also mixed species of Glomus clarum, G. etunicatum, G. manihotis and Gigaspora margarita [82]. Since P uptake is one of the nutrients, most affected by AM symbiosis, in mycorrhizal-legume plants the enhanced P concentration, especially during the seedling and reproductive stages can be very beneficial to the host plant. AM symbiosis is most effective in soils where the amount of available P is at low or medium levels. The data regarding the effect of AM on micronutrients uptake when in a tripartite symbiosis with rhizobium and legumes is very few. However, AM and rhizobium inoculation increased the uptake of Zn and Cu, hyphal colonization, nodule dry weight, N uptake, fixed N and P uptake [78]. Most researches regarding the effects of AM symbiosis on plant growth have been conducted under controlled and greenhouse conditions, and there have been few researches regarding the effects of AM symbiosis on plant growth under field conditions. Hence, it is very necessary to develop non-mycorrhizal legumes mutants so that the effects of inoculated AM in the presence of local AM on legumes plants can also be exactly elucidated under field conditions. The mutants that have been developed so far have not been very applicable, because the mutated gene in the mutants (MYC) controls both the AM symbiosis and the nodule formation (nod) [7]. The other very important point is the recognition role of signal molecules such as flavonoid biochemicals that can have on AM and bacteria and legumes
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symbiosis [24, 25, 78, 79, 83, 84]. For example, the signal molecule formononetin is commercially available and has been indicated to be very effective on AM symbiosis [7, 84]. There are common legume plant genes and biochemical molecules affecting the tripartite symbiosis of the legume host plant with AM and N-fixing bacteria. The presence of a tripartite symbiosis in legumes indicates that legumes have some kind of genetical controlling processes that make this kind of symbiosis likely [85]. There are some pea mutants (Pisum sativum L.) that are not able to develop symbiosis with both AM and N-fixing bacteria. There are stages in both symbioses, controlled by the same genes including hyphal passage into the plant roots by appressorium (Myc1), the development of arbuscule and AM development rate [85, 86].

Effects of Bacteria on P Utilization by AM

Plant P transporters are located in the periarbuscular membrane. Scientists have already cloned the cDNAs from the roots of M. truncatula, which are able to activate P transporters. However, such cDNAs are not expressed in mycorrhizal roots indicating the P transporters that they are active in P uptake under nonsymbiotic conditions only [87]. There are some bacteria, soil P solubilizing bacteria, in the soil that are able to enhance P uptake by AM and plant through enhancing the solubility of soil P, present in organic and inorganic matter. Organic and inorganic P is made available by phosphatase and organic acid producing bacteria, respectively. This significantly increases P uptake by AM hypha and hence the symbiotic host plant [60]. Soil inorganic form of P, which is not available to plants, is strongly bound in the insoluble structures of P and also is attached to the clay surface layers. The synergistic effects of AM and soil solubilizing P bacteria has been indicated by different researches [88]. Under limited availability of soil P, the interaction effects between P solubilizing bacteria and AM result in the enhanced plant colonization by the host plant and the increased bacterial population in the rhizosphere. The coinoculation of AM and P solubilizing bacteria increased plant N and P uptake, relative to control plants [39].

Symbiosis and Signaling

The symbiosis of AM and N-fixing bacteria with the host plants are the most important mutual symbiosesagriculturally and ecologically [54]. For the onset of symbiosis between the host plants and microbes the exchange of signal molecules is necessary [24, 25]. Signal molecules are biochemical compounds stimulating the activity of different genes, involved in the process of symbiosis. Symbiotic bacteria or AM spores realize the presence of the host plant in the
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soil through the secretion of these molecules by the plant roots. Accordingly, the symbiotic bacteria make a chemotactic move to the roots and the spores begin to germinate. However, the spores may also germinate in the absence of the host plant, but they are not able to proceed with the following stages of symbiosis. The stimulated genes of symbiotic bacteria (nodulation genes, NOD, regulated by the transcriptional factor NodD) produce some signal molecules, called lipo-chito-oligosaccharides, which alter the cell cycling in the cortex of plant roots cells and hence resulting in morphological and physiological changes and eventually nodule formation [24, 25, 57]. Although because of the differences in host specificity between bacteria and AM the responses of the two symbionts are different, scientists have found that there are many common stages between bacterial and AM symbioses with the host plant including the exchange of signal molecules [54]. For example, as previously mentioned, there are identical genes in both symbioses that are activated during the symbiosis [89]. In addition, some of the signal molecules necessary for the AM-plant symbiosis have been recently identified [26]. There should be more than a single gene for the perception of Nod (bacteria) and Myc (AM) factors. Because, rhizobium and AM result in different responses, including morphological and although both factors induce similar genes, Nod factors require some extra genes for inducing responses in the host plant. Accordingly, Nod and Myc factors induce genes in different parts of the plant root including epidermis and cortex, respectively, indicating that different plant receptors perceive Nod and Myc factors. Thus the two factors must result in the activation of different pathways in the plant [54]. Since legumes are able to develop symbiotic association with both N-fixing bacteria and AM, they are ideal for the study of the common stages of symbiosis between the two symbionts [90].

Conclusion
Accordingly, the following conclusions may be drawn. The great importance of the interactions among the host plant AM and soil bacteria taking place in soil is more indicated. These interactions must be clearly elucidated as they can have some very significant implications in agriculture and ecology. In addition to their individual functioning in the soil the combined effects of soil microbes are also very important as for example for the production of bioinoculants or their enhancing effects on soil structure and plant nutrients uptake can increase plant growth and hence crop yield. So future research may focus more precisely on the interactions between the host plant, AM and soil bacteria for the more efficient use of soil microorganisms for the development of very advanced agricultural strategies.

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